*Robert M. Levin PhD, Li-Xia, Wu Wei, Catherine Schuler, Robert E. Leggett, Alpha D-Y Lin MD
Effects of Ganoderma Lucidum on Biochemical Dysfunctions of the Rabbit Urinary Bladder using an In-Vitro Model of Ischemia / Reperfusion
Co-Authors
Article Reviewed By:
Ulrike Lindequist(lindequi@uni-greifswald.de)
SIVAKUMAR MANICKAM(Sivakumar.Manickam@nottingham.edu.my)
Citation
Robert M. Levin PhD, Li-Xia, Wu Wei, Catherine Schuler, Robert E. Leggett, Alpha D-Y Lin MD, Effects of Ganoderma Lucidum on Biochemical Dysfunctions of the Rabbit Urinary Bladder using an In-Vitro Model of Ischemia / Reperfusion(2017)SDRP Journal of Plant Science 2(2):65-72
Abstract
Background: Oxidative stress involving ischemia followed by reperfusion are major etiological factors in obstructive bladder dysfunction in both men and rabbits. Specific natural products such as Ganoderma lucidum with significant antioxidant activity have proven to be useful in their treatment. In two recent studies we demonstrated that pretreatment with Ganoderma was effective preventing bladder dysfunction using both in-vivo and in-vitro models of ischemia-reperfusion. The current study is a follow-up study using the in-vitro model of ischemia-reperfusion.
Methods: Eight New Zealand White rabbits were divided into 2 groups. One group (Group-1) was fed Ganoderma (100 mg/Kg) daily for 3 weeks while the other group (Group-2) were given saline. At the end of a 3 week period, each rabbit was euthanized and the bladder separated into twelve full thickness strips and mounted in individual baths. After 1 hour in oxygenated Tyrodes with glucose, 4 strips from each group were removed frozen and stored at -80oC. At this time, the oxygenated Tyrodes + glucose were changed to Tyrodes equilibrated with nitrogen in the absence of glucose (ischemia) for 1 hour. After 1 hour of ischemia the buffer was then changed back to normal oxygenated Tyrode’s with glucose and allowed to recover for 2 hours (reperfusion). After this time period, the four remaining strips from each group were frozen and stored. The isolated strips were analyzed for the following biomarker enzymes: citrate synthase (mitochondria), calcium ATPase (intracellular calcium movement through the cell wall), and sarco-endoplasmic reticular ATPase (intracellular calcium uptake into the sarcoplasmic reticulum following stimulation.
Results: Ischemia-reperfusion resulted in a significant decrease (~50%) in all three enzyme activities. Pretreating with Ganoderma protected all three enzyme activities which were approximately at control levels.
Conclusion: Pretreatment of rabbits for three weeks with Ganoderma prior to subjecting them to in-vitro ischemia-reperfusion significantly protected the bladder enzymes.
References
Sovari, A.A., Cellular and Molecular Mechanisms of Arrhythmia by Oxidative Stress. Cardiol Res Pract, 2016. 2016: p. 9656078. PMid:26981310
PubMed/NCBIDhalla, N.S., et al., Evidence for the role of oxidative stress in acute ischemic heart disease: a brief review. Can J Cardiol, 1999. 15(5): p. 587-93. PMid:10350670
PubMed/NCBIReddy, S. and D. Bernstein, Molecular Mechanisms of Right Ventricular Failure. Circulation, 2015. 132(18): p. 1734-42. PMid:26527692
View Article PubMed/NCBINikooyeh, B. and T.R. Neyestani, Oxidative stress, type 2 diabetes and vitamin D: past, present and future. Diabetes Metab Res Rev, 2016. 32(3): p. 260-7. PMid:26409185
View Article PubMed/NCBIRani, V., et al., Oxidative stress and metabolic disorders: Pathogenesis and therapeutic strategies. Life Sci, 2016. 148: p. 183-93. PMid:26851532
View Article PubMed/NCBIStone, J.R. and L.R. Wilkins, Acute mesenteric ischemia. Tech Vasc Interv Radiol, 2015. 18(1): p. 24-30. PMid:25814200
View Article PubMed/NCBIStoney, R.J. and C.G. Cunningham, Acute mesenteric ischemia. Surgery, 1993. 114(3): p. 489-90. PMid:8367801
PubMed/NCBIBhattacharyya, A., et al., Oxidative stress: an essential factor in the pathogenesis of gastrointestinal mucosal diseases. Physiol Rev, 2014. 94(2): p. 329-54. PMid:24692350
View Article PubMed/NCBINastos, C., et al., Global consequences of liver ischemia/reperfusion injury. Oxid Med Cell Longev, 2014. 2014: p. 906965. PMid:24799983 PMCid:PMC3995148
PubMed/NCBITucker, P.S., A.T. Scanlan, and V.J. Dalbo, Chronic kidney disease influences multiple systems: describing the relationship between oxidative stress, inflammation, kidney damage, and concomitant disease. Oxid Med Cell Longev, 2015. 2015: p. 806358. PMid:25861414
PubMed/NCBITamma, G. and G. Valenti, Evaluating the Oxidative Stress in Renal Diseases: What Is the Role for S-Glutathionylation? Antioxid Redox Signal, 2016. PMid:26972776
View Article PubMed/NCBIJuan, Y.S., et al., The effect of partial bladder outlet obstruction on carbonyl and nitrotyrosine distribution in rabbit bladder. Urology, 2007. 70(6): p. 1249-53. PMid:18158070
View Article PubMed/NCBILi, H.T., et al., Differential effects of coenzyme Q10 and alpha-lipoic acid on two models of in vitro oxidative damage to the rabbit urinary bladder. Int Urol Nephrol, 2011. 43(1): p. 91-7. PMid:20533089
View Article PubMed/NCBINomiya, M., K.E. Andersson, and O. Yamaguchi, Chronic bladder ischemia and oxidative stress: new pharmacotherapeutic targets for lower urinary tract symptoms. Int J Urol, 2015. 22(1): p. 40-6. PMid:25339506
View Article PubMed/NCBILevin, R.M., et al., Partial outlet obstruction in rabbits: duration versus severity. Int J Urol, 2013. 20(1): p. 107-14. PMid:23050656
View Article PubMed/NCBIJuan, Y.S., et al., The beneficial effect of coenzyme Q10 and lipoic acid on obstructive bladder dysfunction in the rabbit. J Urol, 2008. 180(5): p. 2234-40. PMid:18804800
View Article PubMed/NCBILindblom, R., et al., Targeting Mitochondria and Reactive Oxygen Species-Driven Pathogenesis in Diabetic Nephropathy. Rev Diabet Stud, 2015. 12(1-2): p. 134-56. PMid:26676666
View Article PubMed/NCBISaha, S.P. and T.F. Whayne, Jr., Coenzyme Q-10 in Human Health: Supporting Evidence? South Med J, 2016. 109(1): p. 17-21. PMid:26741866
View Article PubMed/NCBIRadu, F., et al., The effect of antioxidants on the response of the rabbit urinary bladder to in vitro ischemia/reperfusion. Mol Cell Biochem, 2011. 355(1-2): p. 65-73. PMid:21541678
View Article PubMed/NCBIKim, J., et al., Phytochemicals in Ischemic Stroke. Neuromolecular Med, 2016. PMid:27193940
View Article PubMed/NCBIXie, C., et al., Persimmon (Diospyros kaki L.) leaves: a review on traditional uses, phytochemistry and pharmacological properties. J Ethnopharmacol, 2015. 163: p. 229-40. PMid:25637828
View Article PubMed/NCBIYu, L., et al., The efficacy and safety of Chinese herbal medicine, Rhodiola formulation in treating ischemic heart disease: a systematic review and meta-analysis of randomized controlled trials. Complement Ther Med, 2014. 22(4): p. 814-25. PMid:25146085
View Article PubMed/NCBIJuan, Y.S., et al., Protective effect of Antrodia camphorata on bladder ischemia/reperfusion injury. Int Urol Nephrol, 2010. 42(3): p. 637-45. PMid:19760512
View Article PubMed/NCBILevin, R.M., et al., Kohki tea protects the rabbit bladder from ischemia/reperfusion-induced contractile dysfunction. Urol Int, 2008. 80(4): p. 425-30. PMid:18587255
View Article PubMed/NCBIFrancis, J.A., et al., Comparative biochemical responses and antioxidant activities of the rabbit urinary bladder to whole grapes versus resveratrol. Mol Cell Biochem, 2015. 410(1-2): p. 121-9. PMid:26354548
View Article PubMed/NCBIFrancis, J.A., et al., Effect of hydrogen peroxide on contractility and citrate synthase activity of the rabbit urinary bladder in the presence and absence of resveratrol and a whole-grape suspension. Mol Cell Biochem, 2014. 391(1-2): p. 233-9. PMid:24627242
View Article PubMed/NCBISuksomboon, N., N. Poolsup, and N. Juanak, Effects of coenzyme Q10 supplementation on metabolic profile in diabetes: a systematic review and meta-analysis. J Clin Pharm Ther, 2015. 40(4): p. 413-8. PMid:25913756
View Article PubMed/NCBIOzkanlar, S. and F. Akcay, Antioxidant vitamins in atherosclerosis--animal experiments and clinical studies. Adv Clin Exp Med, 2012. 21(1): p. 115-23. PMid:23214308
PubMed/NCBILonn, E., Do antioxidant vitamins protect against atherosclerosis? The proof is still lacking*. J Am Coll Cardiol, 2001. 38(7): p. 1795-8. 01626-6
View ArticleMcQuillan, B.M., et al., Antioxidant vitamins and the risk of carotid atherosclerosis. The Perth Carotid Ultrasound Disease Assessment study (CUDAS). J Am Coll Cardiol, 2001. 38(7): p. 1788-94. 01676-X
View ArticleMalone, L., et al., Effect of estrogen and ovariectomy on response of the female rabbit urinary bladder to two forms of in vitro oxidative stress. Int Urogynecol J, 2014. 25(6): p. 791-8. PMid:24346814
View Article PubMed/NCBILin, A.D., et al., Effect of bilateral in vivo ischemia/reperfusion on the activities of superoxide dismutase and catalase: response to a standardized grape suspension. Mol Cell Biochem, 2007. 296(1-2): p. 11-6. PMid:17203243
View Article PubMed/NCBIParekh, M.H., et al., Protective effect of vitamin E on the response of the rabbit bladder to partial outlet obstruction. J Urol, 2001. 166(1): p. 341-6. 66156-3
View ArticleLevin, R.M., et al., Effects of Ganoderma Lucidum shell-broken spore on oxidative stress of the rabbit urinary bladder using an in vivo model of ischemia/reperfusion. Mol Cell Biochem, 2017. PMid:28484937
View Article PubMed/NCBILevin, R.M., et al., Effect of oral Tadenan treatment on rabbit bladder structure and function after partial outlet obstruction. J Urol, 2002. 167(5): p. 2253-9. 65138-5
View ArticleLevin, R.M., et al., Effect of oral Kohki tea on bladder dysfunction induced by severe partial outlet obstruction. J Urol, 2002. 167(5): p. 2260-6. 65139-7
View ArticleMohsin, M., P. Negi, and Z. Ahmed, Determination of the antioxidant activity and polyphenol contents of wild Lingzhi or Reishi medicinal mushroom, Ganoderma lucidum (W.Curt. Fr.) P. Karst. (higher Basidiomycetes) from central Himalayan hills of India. Int J Med Mushrooms, 2011. 13(6): p. 535-44. PMid:22181841
View Article PubMed/NCBIZhao, W., et al., Antioxidant activities of Ganoderma lucidum polysaccharides and their role on DNA damage in mice induced by cobalt-60 gamma-irradiation. Food Chem Toxicol, 2012. 50(2): p. 303-9. PMid:22079311
View Article PubMed/NCBIWong, K.L., et al., Antioxidant activity of Ganoderma lucidum in acute ethanol-induced heart toxicity. Phytother Res, 2004. 18(12): p. 1024-6. PMid:15742340
View Article PubMed/NCBISun, J., H. He, and B.J. Xie, Novel antioxidant peptides from fermented mushroom Ganoderma lucidum. J Agric Food Chem, 2004. 52(21): p. 6646-52. PMid:15479035
View Article PubMed/NCBIYou, Y.H. and Z.B. Lin, [Antioxidant effect of Ganoderma polysaccharide peptide]. Yao Xue Xue Bao, 2003. 38(2): p. 85-8. PMid:12778739
PubMed/NCBIBishop, K.S., et al., From 2000years of Ganoderma lucidum to recent developments in nutraceuticals. Phytochemistry, 2015. 114: p. 56-65. PMid:25794896
View Article PubMed/NCBIBean, H., et al., Antioxidant levels of common fruits, vegetables, and juices versus protective activity against in vitro ischemia/reperfusion. Int Urol Nephrol, 2010. 42(2): p. 409-15. PMid:19768567
View Article PubMed/NCBIHaugaard, N., et al., Effect of partial obstruction of the rabbit urinary bladder on malate dehydrogenase and citrate synthase activity. J Urol, 1992. 147(5): p. 1391-3. 37580-8
View ArticleSpettel, S., et al., Citrate synthase, sarcoplasmic reticular calcium ATPase, and choline acetyltransferase activities of specific pelvic floor muscles of the rabbit. Mol Cell Biochem, 2012. 370(1-2): p. 1-5. PMid:22911511
View Article PubMed/NCBILevin, R.M., et al., Subcellular distribution of SERCA and calcium-activated ATPase in rabbit and human urinary bladder smooth muscle. Pharmacology, 1997. 55(3): p. 136-43. PMid:9346402
View Article PubMed/NCBIRogers, T.B., et al., Use of thapsigargin to study Ca2+ homeostasis in cardiac cells. Biosci Rep, 1995. 15(5): p. 341-9. PMid:8825036
View Article PubMed/NCBIBarry, M., Meigs, JB, The natural history of benign prostatic hyperplasia, in Prostatic Diseases, H. Lepor, Editor. 2000, WB Saunders and Co.: Philadelphia. p. 106-115.
Bushman, W., Etiology, epidemiology, and natural history of benign prostatic hyperplasia. Urol Clin North Am, 2009. 36(4): p. 403-15, v. PMid:19942041
View Article PubMed/NCBIGuven, A., et al., Effect of age on the response to short-term partial bladder outlet obstruction in the rabbit. BJU Int, 2007. 100(4): p. 930-4. PMid:17822471
View Article PubMed/NCBIGuven, A., et al., Effect of aging on the response of biochemical markers in the rabbit subjected to short-term partial bladder obstruction. Mol Cell Biochem, 2007. 306(1-2): p. 213-9. PMid:17673951
View Article PubMed/NCBIGosling, J.A., et al., Correlation between the structure and function of the rabbit urinary bladder following partial outlet obstruction. J Urol, 2000. 163(4): p. 1349-56. 67776-2
View ArticleLevin, R.M., et al., Obstructive response of human bladder to BPH vs. rabbit bladder response to partial outlet obstruction: a direct comparison. Neurourol Urodyn, 2000. 19(5): p. 609-29. 19:5<609::AID-NAU7>3.0.CO;2-H
View ArticleLevin, R.M., et al., Biochemical evaluation of obstructive bladder dysfunction in men secondary to BPH: a preliminary report. Urology, 1999. 53(2): p. 446-50. 00497-X
View ArticleMannikarottu, A., et al., Effect of partial bladder outlet obstruction on nitrotyrosine levels and their correlation with contractile function. Neurourol Urodyn, 2006. 25(4): p. 397-401. PMid:16673378
View Article PubMed/NCBIJuan, Y.S., et al., Coenzyme Q10 protect against ischemia/reperfusion induced biochemical and functional changes in rabbit urinary bladder. Mol Cell Biochem, 2008. 311(1-2): p. 73-80. PMid:18165912
View Article PubMed/NCBIMalone, L., et al., The effect of in vitro oxidative stress on the female rabbit bladder contractile response and antioxidant levels. ISRN Urol, 2013. 2013: p. 639685. PMid:23819065
PubMed/NCBIRadu, F., et al., The effect of in vitro ischemia/reperfusion on contraction, free fatty acid content, phospholipid content, and malondialdehyde levels of the rabbit urinary bladder. Mol Cell Biochem, 2011. 346(1-2): p. 179-86. PMid:20882398
View Article PubMed/NCBIErdem, E., et al., Effect of maturation and aging on response of rabbit bladder to bilateral in vivo ischemia/reperfusion. Urology, 2006. 67(1): p. 220-4. PMid:16413379
View Article PubMed/NCBIBratslavsky, G., et al., Effects of in vivo ischemia on contractile responses of rabbit bladder to field stimulation, carbachol, ATP and KCl. Pharmacology, 1999. 59(4): p. 221-6. PMid:10474082
View Article PubMed/NCBIGill, H.S., et al., The effects of short-term in-vivo ischemia on the contractile function of the rabbit urinary bladder. J Urol, 1988. 139(6): p. 1350-4. 42917-X
View ArticleYamada, A., et al., Persistent overexpression of SERCA2a affects bladder functions under physiological conditions, but not in bladder outlet obstruction-induced sub-acute pathological conditions. J Physiol Sci, 2014. 64(1): p. 21-30. PMid:24037709
View Article PubMed/NCBICallaghan, C.M., et al., The effect of partial outlet obstruction on calpain and phospholipase-2 activities: analyzed by severity and duration. Mol Cell Biochem, 2013. 381(1-2): p. 217-20. PMid:23737136
View Article PubMed/NCBIWang, Y., et al., Effects of mechanical stretch on interstitial cells of Cajal in guinea pig bladder. J Surg Res, 2010. 164(1): p. e213-9. PMid:20828727
View Article PubMed/NCBIZhao, Y., et al., Correlation of ischemia/reperfusion or partial outlet obstruction-induced spectrin proteolysis by calpain with contractile dysfunction in rabbit bladder. Urology, 1997. 49(2): p. 293-300. 00452-9
View ArticleLevin, R.M., et al., Bladder function in experimental outlet obstruction: pharmacologic responses to alterations in innervation, energetics, calcium mobilization, and genetics. Adv Exp Med Biol, 1995. 385: p. 7-19; discussion 75-9. PMid:8571847
View Article PubMed/NCBIStevenson, K., et al., Functional changes in bladder tissue from type III collagen-deficient mice. Mol Cell Biochem, 2006. 283(1-2): p. 107-14. PMid:16444592
View Article PubMed/NCBIEika, B., R.M. Levin, and P.A. Longhurst, Collagen and bladder function in streptozotocin-diabetic rats: effects of insulin and aminoguanidine. J Urol, 1992. 148(1): p. 167-72. 36546-1
View ArticleMonson, F.C., et al., Hyperplasia in the rabbit bladder urothelium following partial outlet obstruction. Autoradiographic evidence. Mol Cell Biochem, 1995. 152(2): p. 167-73. PMid:8751163
View Article PubMed/NCBISantarosa, R., et al., Hyperplasia and apoptosis. Opposing cellular processes that regulate the response of the rabbit bladder to transient outlet obstruction. Lab Invest, 1994. 70(4): p. 503-10. PMid:8176889
PubMed/NCBISalomone, F., J. Godos, and S. Zelber-Sagi, Natural antioxidants for non-alcoholic fatty liver disease: molecular targets and clinical perspectives. Liver Int, 2016. 36(1): p. 5-20. PMid:26436447
View Article PubMed/NCBIKuno, A., M. Tanno, and Y. Horio, The effects of resveratrol and SIRT1 activation on dystrophic cardiomyopathy. Ann N Y Acad Sci, 2015. 1348(1): p. 46-54. PMid:26109180
View Article PubMed/NCBIConte, E., et al., Anti-inflammatory and antifibrotic effects of resveratrol in the lung. Histol Histopathol, 2015. 30(5): p. 523-9. PMid:25515609
PubMed/NCBIJuan, Y.S., et al., Coenzyme Q10 diminishes ischemia-reperfusion induced apoptosis and nerve injury in rabbit urinary bladder. Neurourol Urodyn, 2009. 28(4): p. 339-42. PMid:18837431
View Article PubMed/NCBILasukova, T.V., et al., Cardioprotective Activity of Ganoderma lucidum Extract during Total Ischemia and Reperfusion of Isolated Heart. Bull Exp Biol Med, 2015. 158(6): p. 739-41. PMid:25896590
View Article PubMed/NCBIKan, Y., et al., Antioxidant activity of polysaccharide extracted from Ganoderma lucidum using response surface methodology. Int J Biol Macromol, 2015. 72: p. 151-7. PMid:25149043
View Article PubMed/NCBILiu, S.P., et al., Effects of hypoxia, calcium, carbachol, atropine and tetrodotoxin on the filling of the in-vitro rabbit whole bladder. J Urol, 1998. 160(3 Pt 1): p. 913-9. 62832-5
View ArticleLevin, R.M., et al., Etiology of bladder dysfunction secondary to partial outlet obstruction. Calcium disregulation in bladder power generation and the ability to perform work. Scand J Urol Nephrol Suppl, 1997. 184: p. 43-50. PMid:9165622
PubMed/NCBIZhao, Y., et al., Effect of anoxia on in vitro bladder function. Pharmacology, 1991. 43(6): p. 337-44. PMid:1686111
View Article PubMed/NCBITseng, C.Y., et al., Potent In Vitro Protection Against PM[Formula: see text]-Caused ROS Generation and Vascular Permeability by Long-Term Pretreatment with Ganoderma tsugae. Am J Chin Med, 2016. 44(2): p. 355-76. PMid:27080945
View Article PubMed/NCBIChang, C.J., et al., Ganoderma lucidum reduces obesity in mice by modulating the composition of the gut microbiota. Nat Commun, 2015. 6: p. 7489. PMid:26102296
View Article PubMed/NCBIShen, B., et al., An in vitro study of neuroprotective properties of traditional Chinese herbal medicines thought to promote healthy ageing and longevity. BMC Complement Altern Med, 2013. 13: p. 373. PMid:24373151
View Article PubMed/NCBILai, C.S., et al., Antagonizing beta-amyloid peptide neurotoxicity of the anti-aging fungus Ganoderma lucidum. Brain Res, 2008. 1190: p. 215-24. PMid:18083148
View Article PubMed/NCBICilerdzic, J., et al., Oxidative stress and species of genus Ganoderma (higher Basidiomycetes). Int J Med Mushrooms, 2013. 15(1): p. 21-8. PMid:23510281
View Article PubMed/NCBIWeng, Y., et al., Ganodermasides C and D, two new anti-aging ergosterols from spores of the medicinal mushroom Ganoderma lucidum. Biosci Biotechnol Biochem, 2011. 75(4): p. 800-3. PMid:21512225
View Article PubMed/NCBIWeng, Y., et al., Ganodermasides A and B, two novel anti-aging ergosterols from spores of a medicinal mushroom Ganoderma lucidum on yeast via UTH1 gene. Bioorg Med Chem, 2010. 18(3): p. 999-1002. PMid:20093034
View Article PubMed/NCBISudheesh, N.P., et al., Therapeutic potential of Ganoderma lucidum (Fr.) P. Karst. against the declined antioxidant status in the mitochondria of post-mitotic tissues of aged mice. Clin Nutr, 2010. 29(3): p. 406-12. PMid:20044182
View Article PubMed/NCBIAjith, T.A., et al., Effect of Ganoderma lucidum on the activities of mitochondrial dehydrogenases and complex I and II of electron transport chain in the brain of aged rats. Exp Gerontol, 2009. 44(3): p. 219-23. PMid:19041385
View Article PubMed/NCBI